Evolution of limb development in cephalopod mollusks.

Oscar A Tarazona,Leslie A Slota,Martin J Cohn,Davys H Lopez

doi:10.7554/elife.43828

Abstract

Cephalopod mollusks evolved numerous anatomical novelties, including arms and tentacles, but little is known about the developmental mechanisms underlying cephalopod limb evolution. Here we show that all three axes of cuttlefish limbs are patterned by the same signaling networks that act in vertebrates and arthropods, although they evolved limbs independently. In cuttlefish limb buds, Hedgehog is expressed anteriorly. Posterior transplantation of Hedgehog-expressing cells induced mirror-image limb duplications. Bmp and Wnt signals, which establish dorsoventral polarity in vertebrate and arthropod limbs, are similarly polarized in cuttlefish. Inhibition of Bmp2/4 dorsally caused ectopic expression of Notum, which marks the ventral sucker field, and ectopic sucker development. Cuttlefish also show proximodistal regionalization of Hth, Exd, Dll, Dac, Sp8/9, and Wnt expression, which delineates arm and tentacle sucker fields. These results suggest that cephalopod limbs evolved by parallel activation of a genetic program for appendage development that was present in the bilaterian common ancestor.

Highlights

Animal appendages have widely varying morphologies and perform a multitude of functions, including locomotion, feeding, and reproduction (Nielsen, 2012; Ruppert et al, 2004)
To test the hypothesis that cephalopod limbs evolved by recruitment of an ancient gene regulatory network for appendage development that is conserved across Bilateria, we investigated arm and tentacle development in embryos of the cuttlefish, Sepia officinalis
Our finding that the proximodistal, dorsoventral, and anteroposterior axes of cuttlefish limb buds are patterned by the same pathways that regulate arthropod and vertebrate limb development suggests that the independent evolution of limbs in cephalopod mollusks involved recruitment of an ancient genetic program for appendage development

Summary

Introduction

Animal appendages have widely varying morphologies and perform a multitude of functions, including locomotion, feeding, and reproduction (Nielsen, 2012; Ruppert et al, 2004). Limbs evolved on multiple occasions, and the absence of shared ontogenetic or morphological precursors of appendages in many animal lineages is consistent with their independent origins (Minelli, 2003; Pueyo and Couso, 2005; Shubin et al, 1997) This has led to the view that appendages in different clades of Bilateria are non-homologous morphological innovations that arose by convergent evolution (Nielsen, 2012; Ruppert et al, 2004). A major obstacle to resolving this question is that the evidence of a conserved program derives almost exclusively from Ecdysozoa and Deuterostomia (Pueyo and Couso, 2005; Shubin et al, 1997), and little is known about molecular mechanisms of limb development in Spiralia, the third major superphylum of Bilateria (Grimmel et al, 2016; Prpic, 2008; Winchell and Jacobs, 2013; Winchell et al, 2010)

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Conclusion